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Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress

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Abstract

Trehalose is a nonreducing sugar composed of two glucose units linked in an α,α-1,1-glycosidic linkage. Present in a wide variety of organisms, this sugar may serve as a source of energy and carbon and as a protective molecule against abiotic stresses. In this study, trehalose-producing transgenic rice plants (Oryza sativa) expressing a bifunctional fusion enzyme TPSP (Ubi1:TPSP) were utilized to dissect the enigmatic role of trehalose in conferring stress tolerance to plants. Grown under normal conditions, the Ubi1:TPSP plants produced high amounts of soluble sugars (glucose, fructose and sucrose), ranging from 1.5- to 3.5-fold over NT controls. In the time course of drought treatment, the transcripts for the drought degradable-marker genes (RbcS, FBPase, and PBZ1) persisted for two more days in Ubi1:TPSP plants before being completely degraded relative to those in NT plants, confirming the tolerance of the transgenic plants to drought. This was further supported by a delayed increase in transcript levels of the stress-inducible genes SalT, Dip1, and Wsi18 during drought stress. Similarly, Ubi1:TPSP plants showed tolerance to salt levels of up to 150 mM NaCl, as evidenced by the seedling growth and the delayed decay in RbcS and delayed increase in SalT transcript levels. The growth of NT plants was found to be slightly affected by exogenous trehalose feeding, whereas Ubi:TPSP plants remained resistant, validating the protective role of internally produced trehalose. These results suggest that the elevated production of trehalose in rice, through TPSP overexpression, increases the soluble sugar contents and enhances tolerance to both drought and salt stress.

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References

  • Avigad G, Dey P (1997) Carbohydrate metabolism: storage carbohydrates. In: Dey P, Harborne J (eds) Plant biochemistry. Academic, New York, pp 137–157

  • Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signaling. Nature 449:938–942

    Article  Google Scholar 

  • Claes B, Dekeyser R, Villarroel R, Van de Bulcke M, Bauw G, Van Montagu M, Caplan A (1990) Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant cell 2:19–27

    Article  PubMed  CAS  Google Scholar 

  • Cortina C, Culiáñez-Macià FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75–82

    Article  CAS  Google Scholar 

  • Garcia AB, Engler JDA, Iyer S, Gerats T, Montagu MV, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169

    Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Google Scholar 

  • Goddijn OJM, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4(8):315–319

    Google Scholar 

  • Goddijn OJM, Verwoerd TC, Voogd E, Krutwagen RWHH, de Graaf PTHM, Poels J, van Dun K, Ponstein AS, Damm B, Pen J (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113:181–190

    Article  PubMed  CAS  Google Scholar 

  • Hanson J, Smeekens S (2009) Sugar perception and signalling—an update. Curr Opin Plant Biol 12(5):562–567

    Article  PubMed  CAS  Google Scholar 

  • Holmstrom KO, Mantyla E, Welin B, Mandal A, Palva ET, Tunnnela OE, Londesborough J (1996) Drought tolerance in tobacco. Nature 379:683–684

    Article  Google Scholar 

  • Iturriaga G, Suárez R, Nova-Franco B (2009) Trehalose metabolism: from osmoprotection to signalling. Int J Mol Sci 10:3793–3810

    Article  PubMed  CAS  Google Scholar 

  • Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, Kim YS, Seo HS, Choi YD, Nahm BH, Kim JK (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524

    Article  PubMed  CAS  Google Scholar 

  • Jung H, Kim JK, Ha SW (2011) Use of animal viral IRES sequence makes multiple truncated transcripts without mediating polycistronic expression in rice. J Korean Soc Appl Bi 54(5):678–684

    Article  CAS  Google Scholar 

  • Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose-6-phodphate regulates starch synthesis via posttranslation redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102:1118–11123

    Article  Google Scholar 

  • Miranda JA, Avonce N, Suárez R, Thevelein JM, Van Dijck P, Iturriaga G (2007) A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421

    Article  PubMed  CAS  Google Scholar 

  • Müller J, Wiemken R, Aeschbacher R (1999) Trehalose metabolism in sugar sensing and plant development. Plant Sci 147:37–47

    Article  Google Scholar 

  • Penna S (2003) Building stress tolerance through over-producing trehalose in transgenic plants. Trends Plant Sci 8(8):353–357

    Article  Google Scholar 

  • Pilon-Smits EAH, Terry N, Sears T, Kim H, Zayed A, Hwang S, van Dun K, Vooged E, Verwoerd TC, Krutwagen RW (1998) Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J Plant Physiol 152:525–532

    Article  CAS  Google Scholar 

  • Redillas MC, Kim YS, Jeong JS, Strasser RJ, Kim J-K (2011a) The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10. Plant Biotechnol Rep 5:169–176

    Article  Google Scholar 

  • Redillas MCF, Jeong JS, Strasser RJ, Kim YS, Kim JK (2011b) JIP analysis on rice (Oryza sativa cv Nipponbare) grown under limited nitrogen conditions. J Korean Soc Appl 54(5):827–832

    Article  CAS  Google Scholar 

  • Rolland F, Baena-González E, Sheen J (2006) Sugar sensing and signalling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Romero C, Belles JM, Vaya JL, Serrano R, Culianez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants; pleiotropic phenotypes include drought tolerance. Planta 201:293–297

    Article  PubMed  CAS  Google Scholar 

  • Seo HS, Kyoo YJ, Lim YJ, Song JT, Kim CH, Kim J-K, Lee JS, Choi YD (2000) Characterization of a bifunctional fusion enzyme between trehalose 6-phosphate synthase and trehalose 6-phosphate phosphatase of Escherichia coli. Appl Environ Microbiol 66:2484–2490

    Google Scholar 

  • Stitt M, Lilley RMC, Gerhardt R, Heldt HW (1989) Determination of metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol 174:518–522

    Article  CAS  Google Scholar 

  • Suárez R, Calderón C, Iturriaga G (2009) Improved tolerance to multiple abiotic stresses in transgenic alfalfa accumulating trehalose. Crop Sci 49:1791–1799

    Article  Google Scholar 

  • Wingler A (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60:437–440

    Article  PubMed  CAS  Google Scholar 

  • Yeo ET, Kwon HB, Han SE, Lee JT, Ryu JC, Byun MO (2000) Genetic engineering of drought resistant potato plants by introduction of trehalose-6-phosphate synthase (TPS1) gene from Saccharomyces cerevisiae. Mol Cells 10:263–268

  • Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–1871

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Rural Development Administration under the Cooperative Research Program for Agriculture Science & Technology Development (project no. PJ906910), the Next-Generation BioGreen 21 Program (project no. PJ007971 to J.-K.K.), and by the Ministry of Education, Science and Technology under the Mid-career Researcher Program (project no. 20100026168 to J.-K.K.).

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Authors and Affiliations

  1. School of Biotechnology and Environmental Engineering, Myongji University, Yongin, 449-728, Korea

    Mark C. F. R. Redillas, Su-Hyun Park, Youn Shic Kim, Jin Seo Jeong, Harin Jung, Seung Woon Bang & Ju-Kon Kim

  2. Plant Metabolism Research Center, Graduate School of Biotechnology, Kyung-Hee University, Suwon, 449-701, Korea

    Jang Wook Lee & Tae-Ryong Hahn

Authors
  1. Mark C. F. R. Redillas
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  2. Su-Hyun Park
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  6. Harin Jung
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  9. Ju-Kon Kim
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Correspondence to Ju-Kon Kim.

Additional information

M. C. F. R. Redillas and S.-H. Park contributed equally to this work.

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Redillas, M.C.F.R., Park, SH., Lee, J.W. et al. Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnol Rep 6, 89–96 (2012). https://doi.org/10.1007/s11816-011-0210-3

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  • DOI: https://doi.org/10.1007/s11816-011-0210-3

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